The fine structure of the embryonic envelopes before and after hatching in bothriocephalids: physiological and ecological significance

Abstract

The fine structure and differentiation of the embryonic envelopes before and after hatching in two bothriocephalid species of teleostean fish are described. Scanning electron microscopic observation of the egg surface confirmed the specific ornamentation of the capsule. Its thickness and topographic morphology reflect the physiocochemical characteristics of the environment. Beneath the eggshell, two syncytial layers were observed around the oncosphere. The outer envelope, visible during the preoncospheral phase, degenerated before the liberation of the coracidium. Glycoconjugate labelling confirmed the nutritive character of this layer. After hatching, the inner envelope was the only layer covering the oncosphere. The apical plasma membrane of the coracidial sheath bore cilia and numerous clublike microvilli. Beneath the cortical zone, the syncytial cytoplasm was vacuolated, resembling a honeycomb; the electron-dense zone, described from other pseudophyllideans, was not present. The basal membrane of the inner envelope, uniformly electron-dense, was assimilated by the oncospheral membrane. Comparison of the composition of the embryonic envelopes of pseudophyllideans with those of other tapeworm orders and trematodes revealed ontogenetic, structural and functional similarities between the embryotrophic layers. The physiological and ecological significance of the structure of the free-swimming coracidium is discussed. In this respect, the inner envelope around the oncosphere appears to be responsible for the inability of the larva to detect and invade the intermediate host. Free-swimming larvae are numerous and have been extensively studied in the turbellarians (Tyler 1984) and most of the platyhelminths (Lyons 1977; Threadgold 1984), whereas they are relatively rare in the tapeworm orders, where they are found only in pseudophyllidean (Bothriocephalidae, Haplobothriidae, Triaenophoridae, Dibothriocephalidae, Cephalochylamididae and Amphicotylidae) and trypanorhynchan cestodes (Ubelaker 1983).

Despite the exceptional character of these larvae, which are further distinguished by the early release of the eggs into the outside environment, few studies have dealt with them; even fewer have focused on the embryonic envelopes surrounding the oncosphere during development in the egg and following hatching. The only studies in the literature concernDiphyllobothrium dendriticum (Grammeltvedt 1973),Spirometra mansonoides (Lumsden et al. 1974) andBothriocephalus clavibothrium (Swiderski and Mokhtar 1974; Gabrion 1981 a) and essentially concern the development of the oncosphere tegument.

During experimental studies on hatching and coracidium behavior (Berrada-Rkhami 1984), we considered the possibility of investigating the embryonic envelopes of two bothriocephalid species before and after hatching to determine their physiological and ecological significance. This was the objective of the present study, in which we also compared the structure and evolution of these embryonic envelopes with those of other platyhelminths.